Abstract
Central nervous system neurons become postmitotic when radial glia cells divide to form neuroblasts. Neuroblasts may migrate away from the ventricle radially along glia fibers, in various directions or even across the midline. We present four cases of unusual migration that are variably connected to either pathology or formation of new populations of neurons with new connectivities. One of the best-known cases of radial migration involves granule cells that migrate from the external granule cell layer along radial Bergman glia fibers to become mature internal granule cells. In various medulloblastoma cases this migration does not occur and transforms the external granule cell layer into a rapidly growing tumor. Among the ocular motor neurons is one unique population that undergoes a contralateral migration and uniquely innervates the superior rectus and levator palpebrae muscles. In humans, a mutation of a single gene ubiquitously expressed in all cells, induces innervation defects only in this unique motor neuron population, leading to inability to elevate eyes or upper eyelids. One of the best-known cases for longitudinal migration is the facial branchial motor (FBM) neurons and the overlapping inner ear efferent population. We describe here molecular cues that are needed for the caudal migration of FBM to segregate these motor neurons from the differently migrating inner ear efferent population. Finally, we describe unusual migration of inner ear spiral ganglion neurons that result in aberrant connections with disruption of frequency presentation. Combined, these data identify unique migratory properties of various neuronal populations that allow them to adopt new connections but also sets them up for unique pathologies.
Highlights
Most central nervous system (CNS) neurons become postmitotic near either the ventricle or the pia mater of the brain, typically through the cell division of a radial glia cell, whereas all peripheral nervous system (PNS) neurons are derived either from neural crest or peripheral placodes (Reiprich and Wegner, 2015; Allen and Lyons, 2018)
A process is extended and the nucleus translocates within this leading process either along radial glia fibers or criss-crossing through the radial glia fibers (Fritzsch and Northcutt, 1993) possibly interacting with other glia cells, including oligodendrocytes (Allen and Lyons, 2018) or Schwann cells (Bixby et al, 1988; Lilien and Balsamo, 2005)
A classical example of such migration along radial glia fibers is the migration of cerebellar granule cells along radial Bergman glia fibers from the external granule layer to the internal granule cells (Horn et al, 2018), leaving rarely a few so called “ectopic granule cells” in the external granule cell layer (Frotscher, 1997)
Summary
Most central nervous system (CNS) neurons become postmitotic near either the ventricle or the pia mater of the brain, typically through the cell division of a radial glia cell, whereas all peripheral nervous system (PNS) neurons are derived either from neural crest or peripheral placodes (Reiprich and Wegner, 2015; Allen and Lyons, 2018). Some ocular motor neurons and some inner ear efferents can translocate within a leading process to the contralateral side, turning the leading process into an extension of the axon as the nucleus and cell bodies translocate across the floor plate (Puelles, 1978; Fritzsch et al, 1995; Simmons et al, 2011; Bjorke et al, 2016; Fritzsch et al, 2017). While neurons connected to the vestibular sensory epithelia translocate within their leading processes to form a ganglion between the ear and the brain, spiral ganglion neurons show less translocation and remain near the sensory epithelium to form a distinct spiral ganglion neuron population within the ear (Yang et al, 2011) This overview shows that various migration trajectories can generate unique neuronal populations that are separated from other populations with closely associated spatial and temporal origins through their final topology and associated unique input and output properties. We will expand on current evidence how those unique migratory properties are affecting their connections and physiology and are involved in certain pathologies
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